Review

Carbohydrate and Fiber Recommendations for Individuals with Diabetes: A Quantitative Assessment and Meta-Analysis of the Evidence
James W. Anderson, MD, FACN, Kim M. Randles, Cyril W. C. Kendall, PhD, FACN, and David J. A. Jenkins, MD, PhD, DSc, FACN Department of Internal Medicine, College of Medicine, and the Graduate Center for Nutritional Sciences, University of Kentucky, Lexington, Kentucky (J.W.A., K.M.R.), the Risk Factor Medical Center, St. Michaels Hospital and Department of Nutrition, University of Toronto, Toronto, CANADA (C.W.C.K., D.J.A.J) Key words: diabetes mellitus, nutrition, dietary fiber, carbohydrate, fiber, meta-analysis
To review international nutrition recommendations with a special emphasis on carbohydrate and fiber, analyze clinical trial information, and provide an evidence-based recommendation for medical nutrition therapy for individuals with diabetes. Relevant articles were identified by a thorough review of the literature and the data tabulated. Fixed-effects meta-analyses techniques were used to obtain mean estimates of changes in outcome measures in response to diet interventions. Most international organizations recommend that diabetic individuals achieve and maintain a desirable body weight with a body mass index of 25 kg/m2. For diabetic subjects moderate carbohydrate, high fiber diets compared to moderate carbohydrate, low fiber diets are associated with significantly lower values for: postprandial plasma glucose, total and low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, and triglycerides. High carbohydrate, high fiber diets compared to moderate carbohydrate, low fiber diets are associated with lower values for: fasting, postprandial and average plasma glucose; hemoglobin A1c; total, LDL-cholesterol, HDL-cholesterol and triglycerides. Low glycemic index diets compared to high glycemic index diets are associated with lower fasting plasma glucose values and lower glycated protein values. Based on these analyses we recommend that the diabetic individual should be encouraged to achieve and maintain a desirable body weight and that the diet should provide these percentages of nutrients: carbohydrate, 55%; protein, 1216%; fat, 30%; and monounsaturated fat, 1215%. The diet should provide 2550 g/day of dietary fiber (1525 g/1000 kcal). Glycemic index information should be incorporated into exchanges and teaching material.

Key teaching points:

Medical nutrition therapy is the cornerstone to diabetes management. For obese type 2 diabetic persons, weight management is the most important task with a goal of achieving a body mass index of 25 kg/m2. The most effective diabetes diet, based on a detailed review and meta-analysis of the literature, is a higher carbohydrate, higher fiber diet.

Address correspondence to: James W. Anderson, MD, VA Medical Center (111C), Cooper Drive Room B402, Lexington, KY 40506-2142. E-mail jwandersmd@aol.com Dr. Anderson discloses the following information: GRANTS/RESEARCH SUPPORT (2002-03): NIH, VA, HCF Nutrition Fdn., Abbott, Andryx, Amylin, Astra-Zenica, Aventis, Bristol-Myers Squibb, Dupont Protein Technologies, GlaxoSmithKline, Health Management Resources, Johnson & Johnson, Merck, Novartis, Novo Nordisk, NutriPharma, Procter & Gamble, Regeneron, Roche, Sanofi, Schering Plough, Slim Fast, Weight Watchers, Wyeth-Ayerst. CONSULTANT (2002-03): Bristol-Myers Squibb, Dupont Protein Technologies, GlaxoSmithKline, Health Management Resources, Johnson & Johnson, Nutricia, NutriPharma. HONORARIA (2002-03): Abbott, Bristol-Myers Squibb, Dupont Protein Technologies, GlaxoSmithKline, Merck, Nutricia, NutriPharma, Slim Fast. Dr. Kendall discloses the following information: GRANTS/RESEARCH SUPPORT (2002-03): Heart and Stroke Foundation of Canada, NSERC Canada, Unilever, Loblaw Brands Ltd., National Starch, Protein Technologies, Almond Board of California, International Nut Council, Quaker, Ceapro, Hain-Celestial Group. Dr. Jenkins discloses the following information: GRANTS/RESEARCH SUPPORT (2002-03): Heart and Stroke Foundation of Canada, NSERC Canada, Unilever, Loblaw Brands Ltd., National Starch, Protein Technologies, Almond Board of California, International Nut Council, Quaker, Ceapro, Hain-Celestial Group. CONSULTANT (2002-03): National Starch, NJ; Metcon, Sweden. HONORARIA (2002-03): Metcon, Unilever, Dupont Protein Technologies, Almond Board of California. SPEAKERS BUREAU: Almond Board of California.

Journal of the American College of Nutrition, Vol. 23, No. 1, 517 (2004) Published by the American College of Nutrition 5

Carbohydrate and Fiber Recommendations in Diabetes

Because of the high risk for atherosclerotic disease, optimal management of lipoproteins, blood pressure and oxidative stress is important. Health-promoting diabetes diets emphasize whole grains, vegetables, fruits, and low glycemic index foods, and soy protein.

Introduction
Diabetes is emerging in epidemic proportion throughout the world [1,2]. Nutritional recommendations for individuals with diabetes mellitus need revision as new information about effects of nutrients on insulin sensitivity, glycemic excursion, serum lipoproteins, and pathophysiology of diabetes mellitus emerge. The medical literature was reviewed and research data were assembled in order to reexamine and prioritize the goals of medical nutrition therapy of diabetes mellitus. We also reviewed recommendations from international diabetes associations and cardiovascular nutrition expert panels. We assessed randomized-clinical trials using quantitative (meta-analysis) techniques to apply this evidence-based knowledge to recommendations about intake of macronutrients and dietary fiber for persons with diabetes. These recommendations also have implications for persons at high risk for developing diabetes. In this review we will focus on these areas: nutrition recommendations from various national diabetes associations and cardiovascular nutrition expert panels, percentage of energy recommended from carbohydrate considering its impact on glycemic control and serum lipoproteins, reevaluation of amount of dietary fiber to be recommended and updated assessment of the glycemic index and its potential role in nutrition management.

use of the glycemic index. The British and Canadian Associations recommend moderation in protein intake while others have recommended ranges that are similar to those for the general population. Total fat intake is usually limited to 30% of energy with an emphasis on restriction of saturated and trans-fatty acids. Moderation in polyunsaturated fat intake is recommended and monounsaturates are the fatty acids of choice. These considerations provide the foundation for this evidence-based review and recommendations.

Macronutrient Considerations
To assess the effects of carbohydrate and fiber intake on glycemic control and serum lipids we have reviewed clinical studies performed over the last 25 years. Studies were identified by a search of MEDLINE and by review of references in relevant research reports and reviews. After tabulating data we calculated effect size expressed as percentage change for each variable and then, using the fixed-effects model for metaanalysis, we calculated variance-adjusted percentage changes as previously described [12,13]. We evaluated all clinical trials that provided glycemic outcome data. Study designs were classified as observational, controlled, randomized, or randomized and controlled trials (RCT). Observational studies presented data before and after dietary intervention. Controlled studies compared the intervention with a control diet. Randomized studies used some form of randomization. RCTs used randomization and control-diet observations. Data from all trials were tabulated and assessed. Where adequate data from RCTs were available, these data were analyzed using variance-weighted (meta-analysis) methods as previously described [1214]. In some instances, variance-weighted values are presented for all studies. We will use the term variance-weighted values to represent mean estimates obtained by the fixed-effects meta-analysis model. The levels of carbohydrate intake were classified as follows: high carbohydrate, 60% of energy; moderate carbohydrate, 30% to 59.9% of energy; low carbohydrate, 30% of energy. The levels of fiber were classified as follows: high fiber, 20g/1000 kcal; moderate fiber, 10 to 19.9 g/1000 kcal; and low fiber, 10 g/1000 kcal. To estimate recommended ranges for nutrients we averaged lower and higher values recommended for each nutrient. When a specific recommendation (e.g., 60% of energy from carbohydrate) was given and a range was not provided we calculated the mean range from available data and added and subtracted half the range for the recommended value. For example, the mean range for carbohydrate from lowest to highest recommended values from seven associations was 9.3%. Half the range was 4.65%, which was rounded to 5%. Thus, we added

International Nutrition Recommendations for Persons with Diabetes

Nutrition recommendations for persons with diabetes are available from the American Diabetes Association [3], British Diabetes Association [4], Canadian Diabetes Association [5], European Association for the Study of Diabetes [6], as well as from India [7], Japan [8] and South Africa [9]. Because of the concern about CHD for persons with diabetes the recent recommendations of the American Heart Association [10] and the National Cholesterol Education Panel (Adult Treatment Panel 3) [11] were also considered. All of these recommendations are summarized in Table 1. Recommendations from the international community are similar except for those regarding overweight and obesity. Six of the nine groups recommend weight loss to a desirable weight with recommendations to achieve and maintain a body mass index (BMI) of 25 kg/m2. Most diabetes authorities recommend a carbohydrate intake of 50 60% of energy. They emphasize whole grains, vegetables, fruits, and dry beans. While most diabetes associations have specific restrictions on sugar intake, the American Diabetes Association does not emphasize restriction of sugars [3]. Most authorities recommend an increase in dietary fiber intake while there is not a consensus on

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

Table 1. International Recommendations for Medical Nutrition Therapy for Persons with Diabetes
Parameter Weight Reduction ADA [3] Modest weight loss (57%) 5060% BDA [4] BMI to approach desirable weight 5055% CDA [5] Maintain healthy weight (710%) 5060% EASD [6] BMI 18.525 desirable weight 4560% (55 60% with low GI foods) Low GI foods Japan [8] Attain & maintain desirable weight 60% S Africa [9] Achieve & maintain reasonable weight 5560% India [7] 1923 BMI desirable weight 65% AHA [10] Achieve & maintain desirable weight 4555% NCEP [11] Maintain desirable weight 5060%

Carbohydrate

Polysaccharides

Whole grains, fruits, vegetables

Most of CHO, rich in fiber or resistant starch 25 g/d

Whole grain cereals & legumes

Vegetables300 g

Whole grain cereals & legumes

Mono- & Disaccharides Glycemic index

No restriction Does not recommend for general use As for general population 1520% 2535% 10% 1020% 10% 300 mg/d

10% added Includes low GI foods 2535 g/d

10% calories

1 serving fruit

Discusses

Fiber, total

30 g/d

Protein Total fat Saturated/Trans Fatty Acids Monounsaturated Fatty Acids Polyunsaturated Fatty Acids Cholesterol

1015% 3035% 10% 1015% 10% 300 mg/d

11%, 0.86 g/kg/d 30% 10% 1015% favored 10%

With meals, Recommended low GI foods recommended Increase with 1 fruit, 400 g low GI vegetables foods 1020% 1520% 35% 10% 1020% favored 10% 300 mg 2025%

10% added sugar Quotes supportive references 40 g/d

Vegetables, fruits, legumes 40 g/d; cereal 40 g From foods

Grains, whole grains, fruits, vegetables No comment No comment

No comment

1220% 30% 10% 13% 68%

From fruits, 25 g/d vegetables, legumes 15% 21% 7% 7% 7% 30% 10% 11% 10% 200 mg

2030 g/d

15% 2535% 7% up to 20% up to 10% 200 mg

and subtracted 5% to the specific recommendation to obtain values for range. When a specific recommendation of 60% of energy from carbohydrate was recommended, we expanded this to a range of 55 65%.

Carbohydrate and Dietary Fiber

Twenty-four studies met the inclusion criteria and summary characteristics are presented in Table 2. Eleven studies compared moderate carbohydrate, high fiber (MCHF) to moderate carbohydrate, low fiber diets [1525]. These studies examined the independent effects of dietary fiber on glucose and lipid metabolism; they included an average of 16 subjects and were an average duration of 43 days. Nine of the 11 MCHF studies were RCTs. Thirteen studies (Table 2) examined high carbohydrate, high fiber diets (HCHF) with lower carbohydrate, lower fiber diets [26 38]. These studies examined the effects of increasing

both carbohydrate and fiber in the diet; they enrolled an average of 13 subjects for an average of 29 days. Four of the 13 HCHF studies were RCTs. Because body weight change has an important impact on serum glucose and lipoprotein values [39], we assessed weight change for these studies. Investigators provided weight change information for 18 of the 24 studies; the average subject lost a variance-adjusted 0.58% of initial body weight (95% confidence intervals, 3.7 to 1.6%). Variance-adjusted weight losses were not statistically significant for MCHF diets or HCHF diets and there was not a significant correlation between weight change and fasting plasma glucose changes. In Table 3, the variance-weighted (meta-analysis) MCHF diet effects on serum glucose and lipid values are presented. Only RCTs are included in this table. A meta-analysis using all available studies yielded results consistent with those presented in this table. Compared to control diets, MCHF diets decreased fasting plasma glucose values in 5 of 5 studies reporting this variable but these changes were not statistically significant.

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

Carbohydrate and Fiber Recommendations in Diabetes

Table 2. Descriptive Characteristics of Moderate Carbohydrate, High Fiber and High Carbohydrate, High Fiber Studies
Study Rivellese [15] Rivellese [16] Dodson [17] Karlstrom [18] Riccardi [19] Pacy [20] Pacy [21] Hagander [22] Venhaus [23] Lafrance [24] Chandalia [25] Anderson [26] Anderson [27] Anderson [30] Simpson [28] Simpson [29] Hoffman [31] Ward [32] Taskinen [33] Pacy [34] Story [35] Simpson [36] ODea [37] Anderson [38] Number of Subjects 4 IDDM/4 NIDDM 6 IDDM/8 NIDDM 50 NIDDM 14 NIDDM 6 IDDM/8 NIDDM 3 IDDM/14 NIDDM 11 NIDDM 14 NIDDM 10 IDDM 9 IDDM 13 NIDDM 7 IDDM/3 NIDDM 20 IDDM 10 IDDM/4 NIDDM 9 IDDM 18 NIDDM 7 NIDDM 7 NIDDM 10 IDDM 5 IDDM/20 NIDDM 14 IDDM 13 NIDDM 10 NIDDM 10 IDDM Study Design randomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled observational observational randomized, controlled observational randomized, controlled randomized, controlled controlled controlled controlled randomized, controlled randomized, controlled controlled randomized, controlled controlled controlled controlled observational randomized randomized, controlled Type of Diet MCHF MCHF MCHF MCHF MCHF MCHF MCHF MCHF MCHF MCHF MCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF HCHF Treatment Period (d) 10 10 90 21 10 90 90 56 42 12 42 18 16 1435 42 42 7 42 14 90 1428 18 14 28

Table 3. Results of a Meta-Analysis on Moderate Carbohydrate, High Fiber versus Moderate Carbohydrate, Low Fiber DietsAnalysis of Randomized Controlled Trials
Parameter Fasting Plasma Glucose Postprandial Plasma Glucose Average Daily Plasma Glucose HbA1c Total Cholesterol LDL Cholesterol HDL Cholesterol Triglycerides Number of Studies 5 4 5 4 8 6 8 7 Number of Subjects 59 45 59 62 112 77 112 98 Weighted Average Percent Change 6.0 20.9 5.0 2.5 6.5 7.9 3.9 8.3 LCI 13.8 32.6 11.3 3.2 9.4 12.0 9.0 14.1 UCI 1.8 9.2 1.2 8.1 3.7 3.9 1.3 2.4

Similarly, MCHF diets were associated with lower average daily plasma glucose values in 4 of 5 studies but these changes were not significant. However, MCHF diets were accompanied by lower postprandial plasma glucose values in 5 of 5 studies reporting this variable and these reductions averaging 21% were statistically significant. MCHF diets also significantly decreased total and LDL cholesterol (7% and 8% respectively). These diet insignificantly decreased HDL-cholesterol values by 4%. Values for LDL:HDL-cholesterol ratios were not provided for some studies but the changes can be estimated for the changes in LDLand HDL-cholesterol values and indicate that values decreased 4.5%. MCHF diets significantly decreased fasting serum triglyceride values an average of 8%. In Table 4, a metaanalysis of HCHF diet effects on glucose and lipid values are

presented. Because of the limited number of randomized, controlled trials in this area, all applicable studies were included in this analysis. The analysis of average, unweighted changes for all studies and a meta-analysis using only randomized, controlled trials yielded data that were consistent with those data presented in this table. Compared to baseline measurements, HCHF diets decreased fasting plasma glucose values in all 12 studies and HbA1c in all 6 studies reporting these variables. Thus, HCHF diets were shown to significantly decrease all indicators of glycemia, particularly fasting plasma glucose (14%), postprandial plasma glucose (14%), and average daily plasma glucose (13%). The decrease in HbA1c was also significant. HCHF diets decreased serum cholesterol values in all 12 studies with 10 of the studies reporting significant reductions. HCHF diets reduced all serum lipid measures. Total cholesterol

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

Table 4. Results of a Meta-Analysis on High Carbohydrate, High Fiber versus Moderate Carbohydrate, Low Fiber DietsAll Studies
Parameter Fasting Plasma Glucose Postprandial Plasma Glucose Average Daily Plasma Glucose HbA1c Total Cholesterol LDL Cholesterol HDL Cholesterol Triglycerides Number of Studies 12 3 3 6 11 5 7 9 Number of Subjects 141 47 37 79 146 71 91 119 Weighted Average Percent Change 14.3 13.6 12.5 6.0 19.3 16.4 6.3 12.8 LCI 19.2 24.6 22.0 11.6 22.6 25.2 10.9 21.2 UCI 9.4 2.6 3.0 0.3 15.9 7.7 1.7 4.3

decreased significantly by 19% and LDL-cholesterol decreased significantly by 16%. HDL-cholesterol decreased nonsignificantly by 6%. Importantly, decreases in LDL:HDL-cholesterol values were 10.9%. HCHF diets significantly decreased fasting serum triglyceride levels by 13%.

Comments
These clinical trials indicate that high-fiber, moderate-carbohydrate (MCHF) diets significantly improve glycemic control of diabetic subjects compared to moderate carbohydrate, low-fiber diets. These analyses provide the best estimate of the effects of increasing dietary fiber independent of carbohydrate in the diet of persons with diabetes. Increasing the dietary fiber has the greatest impact on postprandial serum glucose values. The MCHF diets also significantly decrease fasting serum cholesterol, LDL-cholesterol, and triglyceride values. The MCHF diets were accompanied by insignificant decreases of HDL-cholesterol values of 4%. It seems likely that favorable changes in the LDL:HDL cholesterol values and decreases in serum triglycerides would outweigh the unfavorable changes in serum HDL-cholesterol values. Based on previous estimates [39], the reduced serum cholesterol values would decrease CHD risk by 16.4% while the decreased HDL-cholesterol values would increase risk by 11.9%. Of course, the decreased fasting serum triglycerides would further reduce risk for CHD. These low-fiber vs. high-fiber diet comparisons indicate that increasing dietary fiber in the diet of diabetic individuals is likely to improve glycemic control and lower risk for CHD. The high-fiber diets in these studies provided 20 grams of dietary fiber/1000 kcal. High-carbohydrate, high-fiber (HCHF) diets provide even greater benefits on glucose and lipid values for diabetic individuals when compared to low or moderate carbohydrate, low or moderate fiber diets. HCHF diets are accompanied by significant decreases in all aspects of glycemic control including HbA1c. Of course, these benefits result from increases in both carbohydrate and fiber intakes. Earlier studies have documented the glycemic and lipidemic benefits of increases in carbohydrate and decreases in fat intake [38,40,41]. HCHF diets produce even greater reductions in all lipid parameters

including HDL-cholesterol values. However, these diets were lower in saturated fat and cholesterol content than the control diets; decreased saturated fat intake would be expected to lower serum HDL-cholesterol values [42]. Again, the reductions in cholesterol and triglycerides appear to outweigh the decreases in HDL-cholesterol values since the cholesterol reduction would reduce risk by an estimated 48.1% while the HDLreduction would increase risk by 20.1% [39]. Also, the LDL: HDL-cholesterol values were 10.9% lower on the HCHF than control diets. These studies support the argument that increasing carbohydrate content of the diet to 60% of energy and including 20 grams of dietary fiber/1000 kcal. provide distinct benefits on glycemic control and serum lipoprotein values for diabetic individuals. Dietary fiber has many health benefits and addresses the specific health problems of diabetic individuals. In addition to non-specific CHD protective effects [14,43 45], dietary fiber has favorable effects on serum LDL-cholesterol [45 47], triglycerides [48], blood pressure [43], weight management [49] and postprandial glycemia (both first and second meal effects) [50]. Thus, there appear to be many reasons to recommend that diabetic individuals consume more fiber than recommended for the general population. Based on the available data, we recommend that diabetic patients consume a high-carbohydrate, high-fiber, low-fat diet. Overweight individuals, of course, should reduce energy intake and increase physical activity to achieve and maintain a desirable body weight. The available data, as summarized above, suggest that the greatest benefits on glycemic control and serum lipoproteins are achieved with a carbohydrate intake of 60% of energy. The longest studies were 90 days in duration and, therefore, long-term clinical research data on HCHF diets are not available. However, since clinical evidence suggest that long-term benefits can be achieved for diabetic individuals with 55% of energy from carbohydrate [51], we recommend that carbohydrate goals should be 55% with a desirable range of 55 65% of energy to increase the practical application of this dietary change. The potential advantages and disadvantages of substituting monounsaturated fats for carbohydrates is discussed elsewhere [3].

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

Carbohydrate and Fiber Recommendations in Diabetes

The available data indicate that high intakes of dietary fiber (20 grams/1000 kcal) in the setting of moderate or of highcarbohydrate intakes clearly have benefits for glycemic control and serum lipoproteins. In a one-year RCT for dyslipidemic non-diabetic subjects we demonstrated the serum lipid benefits of a diet providing 55% of energy as carbohydrate and 25 grams/day of dietary fiber (13 grams/1000 kcal) [26]. The US National Academy of Sciences Institute of Medicine recently recommended that adult men 50 years and younger consume 38 grams of total dietary fiber daily and women 50 years and younger consume 25 grams of fiber daily. For persons over 50 years the recommendation is for 30 and 21 grams daily for men and women, respectively [52]. Based on the evidence and recommendations from the international diabetes community (Table 1) we recommend a dietary fiber intake of 2550 grams/ day or 1525 grams/1000 kcal. for diabetic individuals. The carbohydrate and fiber guidelines can readily by achieved by following consensus nutrition guidelines. A healthy diet including, for example, 1500 kcal/day from these choices: three servings of whole grains; five other servings of bread, cereal, rice and pasta; one or more serving of beans; four servings of vegetables; three servings of fruit; two servings of low-fat dairy products, two servings of protein; and three servings of fat. With inclusion of other foods not rich in fiber to reach an energy intake of 2000 kcal/day, this intake would provide approximately these amounts of nutrients: carbohydrate, 285 grams (57% of energy), 70 grams of protein (14% of energy), 65 grams of fat (29% of energy) and 42 grams of fiber (21 grams/1000 kcal). Care should be taken not to increase fiber intake predominantly from insoluble sources such as wheat bran since the evidence is not strong that the non-viscous fiber sources benefit glycemic control [53,54] Because of the potential HDL-cholesterol-lowering effect of these diets, these levels should be monitored regularly and diabetic individuals should be encouraged to increase physical activity and, of course, avoid cigarette smoking [10,11]. Choosing lower glycemic index foods may also favorably affect serum HDL-cholesterol values [55,56]. For some individuals, substituting monounsaturated fat for carbohydrate may increase serum HDL-cholesterol values [57]. Foods including nuts, avocado, and olive oil with green vegetables may be particularly useful for inclusion [58].

Glycemic Index
The glycemic index of a food is defined as the ratio of the glycemic response to that food and the glycemic response to a standard food, typically white bread. Consumption of low glycemic index foods results in lower postprandial plasma glucose and a lower insulin response as compared to consumption of high GI foods. The preferential response to low GI foods is seen in both diabetics and nondiabetic individuals. The potential benefits of low GI foods are summarized elsewhere [59,60]. We compiled the results of ten studies comparing the effects of low GI diets and high GI diets in diabetic patients [6170]. The characteristics of these studies are presented in Table 5. Nine of the 10 studies were RCTs. These studies included an average of 14 subjects for a mean duration of 33 days. Recently Brand-Miller has completed a meta-analysis of 14 clinical studies comparing low vs. high glycemic index diets in diabetic individuals [71]. Inclusion criteria for our current analysis and that of Brand-Miller differed so the included studies differed. Her analyses also included data from these studies [24,7276]. We completed a meta-analysis on the data from the nine randomized controlled trials, the results of which are presented in Table 6. Fasting plasma glucose values were significantly lower on low GI diets than high GI diets. Fructosamine and HbA1c were lower with the low GI than the higher GI diets but the differences were not statistically significant. When BrandMiller aggregated the glycated proteins (HbA1c and fructosamine) she noted a significant 7.4% reduction in glycated proteins (95% CI, 8.8 to 6.0) [71]. In our analysis, total cholesterol and LDL-cholesterol values were lower with lower GI than higher GI diets but these changes were not significant. HDL-cholesterol was increased slightly by an average of 3%. The decrease in the LDL:HDL-cholesterol ratio was 8.5%. Our analysis indicates that low GI diets compared to high GI diets are associated with a decrease in serum triglycerides of

Table 5. Descriptive Characteristics of Low GI Diet Versus High GI Diet Studies

Study Jenkins [61] Calle-Pascual [69] Collier [62] Fontvieille [70] Brand [68] Wolever [65] Fontvieille [67] Wolever [66] Jarvi [64] Luscombe [63] Number of Subjects 8 NIDDM 12 IDDM/12 NIDDM 7 IDDM children 8 IDDM 16 NIDDM 6 NIDDM 12 IDDM/6 NIDDM 15 NIDDM 20 NIDDM 21 NIDDM Study Design randomized, controlled nonrandomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled randomized, controlled Treatment Period (d) 14 28 42 21 84 42 35 14 24 28

10

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

Table 6. Meta-Analysis of Responses to Low GI Diets Versus High GI Diets
Parameter Fasting Plasma Glucose Fructosamine HbA1c Total Cholesterol LDL Cholesterol HDL Cholesterol Triglycerides Number of Studies 8 7 4 7 5 8 8 Number of Subjects 104 81 62 97 71 104 104 Weighted Average Percent Change 7.5 2.5 3.3 1.4 5.4 3.4 6.3 LCI 14.5 6.4 8.5 5.2 12.6 2.1 17.4 UCI 0.5 1.5 1.8 2.3 1.8 9.0 4.9

6%. Brand-Miller, in an analysis of 8 studies, reported an average triglyceride reduction of 12% [71]. The non-significance of the decreases in the levels of glycosylated proteins that we observed could have been due to the fact that all but one of the studies involved treatment periods of less than two months.

Comments
Low glycemic index foods represent healthy choices for persons with diabetes or dyslipidemia. Lower GI foods, compared to higher GI foods, decrease fasting and postprandial blood glucose values [60]. These foods decrease serum LDLcholesterol and triglyceride values. Lower GI foods are associated with significantly higher HDL-cholesterol values than higher GI foods [55,56,77]. The health implications of the GI were recently critically reviewed. [78,79]. Liu and colleagues have examined the relationship between high glycemic load and fasting serum HDL-cholesterol, serum triglycerides, risk for CHD, and risk for diabetes [80]. The glycemic load, representing the grams of carbohydrate multiplied by the glycemic index ratio (a food with a GI of 100 has a ratio of 1.0 while a food with a GI of 60 has a ratio of 0.6), is proportional to the GI. Thus, with the same carbohydrate intake, persons with a low glycemic load have a lower GI diet [80]. Persons with a low glycemic load compared to persons with a high glycemic load have significantly higher HDL-cholesterol and significantly lower fasting serum triglyceride values [56]. Persons with the low glycemic load have lower risk for developing diabetes [81,82], but not all studies support this conclusion [83]. A lower glycemic load appears to reduce risk for CHD [84] and lower non-lipid risk factors for CHD [80]. A number of diabetes associations endorse the use of GI information and recommend that low GI foods be incorporated into the diet. For example, Diabetes Australia defines the GI and recommends that the diet include three low GI foods throughout the day, ideally one at each meal; low GI foods are listed in bold in food exchange lists [85]. Other diabetes associations are developing easy-to-use strategies for encouraging use of low GI foods. Brand-Miller lists the following organizations that endorse the use of the GI: FAO/WHO [86], European Association for the Study of Diabetes [87], Diabetes Australia [88], Canadian Diabetes Association [5], German Dietetic Association, South African Diabetes Association and

New Zealand Dietetic Association [71]. Gilbertson and colleagues document that low GI diets are easy to teach, easy to learn for Australian children with type 1 diabetes [75,90]. The many clinical studies we have reviewed and the observational studies almost invariably suggest that lower GI diets provide health benefits, improve glycemic control and favorably alter CHD risk factors. These studies do not suggest harmful or detrimental effects. While we agree that more research is required [89], we conclude that the benefits outweigh the disadvantages for use of low GI food information in counseling. We endorse the recommendations emanating from many national and international diabetes and nutrition organizations and advocate that diabetic individuals be encouraged to show preference to low GI foods and include three low GI foods into their diet daily.

Whole Grains, Vegetables and Fruits

Whole grains, vegetables and fruits are an integral part of the recommended high carbohydrate, high fiber diet. Most whole grain foods are rich sources of insoluble fiber, minerals, antioxidants and other bioactive compounds [91]. Higher intakes of whole grains are associated with protection from CHD [14,92], diabetes [83] and, perhaps, obesity [93]. Diabetes associations and national advisory bodies recommend intake of three servings of whole grain foods per day [94]. The importance of whole grains with its many facets, including the germ and the potential low glycemic index value, may have to be stressed since wheat bran alone may have little effect on blood lipids or glycemic control [54]. Many vegetables and fruits are rich sources of soluble and insoluble fiber, vitamins and minerals. Soluble fiber-rich foods, such as dry beans and whole grain oat and barley products, have important hypocholesterolemic effects [47]. Diabetes associations and national advisory boards recommend intake of a minimum of three servings of vegetables and two servings of fruit per day.

Recommendations
Recommended Ranges from International Organizations. International and US recommendations are tabulated in Table 7 (middle column). These weighted values were determined as described in the Methods section. The international

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

11

Carbohydrate and Fiber Recommendations in Diabetes

Table 7. Evidence-Based Nutrition Recommendations for Persons with Diabetes.
Weighted Values from International Bodies Weight Reduction Carbohydrate Polysaccharides Mono- & Disaccharides Glycemic Index Fiber, Total Protein Total fat SFA/Trans MUS PUFA Cholesterol Glycemic Index Attain & maintain desirable weight (BMI25) 5060% Whole grains, legumes, vegetables 40 g/d, fruits and vegetables Low GI foods favored 2535 g/d 1118% 2530% 10% 914% 9% 200 mg Low GI foods favored Evidence-Based Recommendations Attain & maintain desirable weight (BMI25) 5565% Whole grains, legumes, vegetables Moderation Incorporate GI into exchanges and teaching material 2550 g/d (1525 g/1000 kcal) 1216% 30% 10% 1215% 10% 200 mg/d Incorporate GI into exchanges and teaching material

diabetes community, the AHA and NCEP recommendations are fairly concordant except for weight recommendations. Six of the nine recommendations indicate that achieving and maintaining a desirable weight (BMI 25 kg/m2) is a strong health recommendation. Mann and Lewis-Barned [95], summarizing recommendations for Europe and North America recommend a BMI goal of 25 kg/m2. Because 58% of newly diagnosed Chinese persons with type 2 diabetes are overweight, Pan [96] recommends reducing weight to desirable (BMI 25 kg/m2). The importance of weight management for obese diabetic individuals is reviewed in detail elsewhere [97]. The recommended mean range for total carbohydrate intake is 5060% of energy with an emphasis on whole grains, dry beans and lentils, vegetables and fruits. The general diabetes community recommends that monosaccharides and disaccharides intake be in the moderate range. Three diabetes associations and Diabetes Australia [85] recommend use of the glycemic index and only the American Diabetes Association does not recommend the glycemic index for general use. The recommended mean fiber intake of 2535 grams per day is higher than most populations consume and, thus, represent a recommended increase in fiber intake for persons with diabetes. The US National Academy of Sciences Institute of Medicine [52] recently recommended that men under 50 years of age consume 38 grams of dietary fiber/day and that women under 50 consume 25 grams/day. The recommended mean protein intake represents 1118% of energy. The recommended mean intakes for fats are as follows: total fat, 2530% of energy; saturated plus trans fatty acids, 10%; monounsaturated fatty acids, 914%; and polyunsaturated fatty acids, 9%. The recommended intake for dietary cholesterol is 200 mg/day for diabetic individuals [10,11]. These recommended mean intakes are recommendations from these groups but may not represent values developed from an evidence-based analytical review of the literature. Nevertheless, there is a fairly remarkable similarity across these recommendations. Evidence-Based Recommendations. In this review we have carefully assessed the clinical studies examining issues

regarding macronutrient and fiber intake and applied quantitative analysis using meta-analysis techniques to assess the strength of the evidence for various recommendations. Our recommendations (Table 7, right hand column), where data are available, are based on this process. The major areas of disagreement relate to recommendations regarding weight loss and maintenance, dietary fiber intake, use of the glycemic index, and protein recommendations. Weight gain and obesity are the major contributing factors to development of diabetes [98100]. Weight gain and obesity are major risk factors for development of CHD [39]. Diabetic individuals have a three- to five-fold higher risk for CHD [101] and 80% of diabetic individuals die from atherosclerotic cardiovascular disease [102]. Excessive energy intake and obesity are major contributors to insulin resistance and poor glycemic control [97]. Based on these considerations we recommend that a major nutrition goal is attaining and maintaining a desirable body weight (BMI 25 kg/m2) [97]. Our evidence-based analysis supports recommendations that the total carbohydrate intake be 55% or in the range of 5565% of energy intake. The high-carbohydrate, high-fiber diet extensively and effectively used by Viswanathan and colleagues [103] in Madras, India, for diabetes management has included 67% carbohydrate, 19% protein (predominantly from vegetable sources), and 14% fat with 25 g/1000 kcal of dietary fiber for 40 years. Our clinical impression and longterm clinical observations suggest that the glycemic benefits of higher carbohydrate intakes can be achieved with intakes of 55% of energy [35]. The health benefits of whole grain foods are emerging strongly [14], and the US FDA recently approved a health claim indicating that intake of whole grains as part of a diet lower in saturated fat and cholesterol may reduce risk for CHD [104]. Vegetables are universally endorsed as promoting health and four servings per day are recommended [105]. Only one diabetes association recommends a limitation of fruit intake; we concur with most diabetes associations that fruit intake should not be restricted. We concur with the broad recommendations that added monosaccharides and disaccharides, not from fruit or vegetables, should be used in moderation.

12

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

The extensive data regarding the glycemic and lipidemic benefits of high fiber intakes (as summarized in tables 3 and 4) lead to the conclusion that higher fiber intakes should be recommended for persons with diabetes. Higher fiber intakes improve glycemic control, lower serum cholesterol and LDLcholesterol levels and slightly reduce serum triglyceride values. Fiber intake also reduces risk for CHD [14] and assists in weight management [106]. Based on these observations, we recommend a fiber intake of 2550 grams/day or 1525 grams/ 1000 kcal. These levels can be readily achieved by following general nutrition guidelines for intake of these foods: whole grains, especially oats and barley; whole grain breads, cereals, and pastas; brown rice, dry beans, peas and lentils; nuts; fruits; and vegetables. The glycemic index has been controversial since first introduced [107]. Extensive research indicates that the glycemic index of a meal is a major determinant of postprandial hyperglycemia in nondiabetic and diabetic individuals [59]. The glycemic indices of many foods have been measured and tabulated [108]. Many diabetes associations recommend that the glycemic index be incorporated into nutrition counseling for diabetic individuals (Table 1). The evidence indicates that short-term increases in the intake of low glycemic foods significantly lowers fasting plasma glucose values and produces favorable trends in other glycemic and lipidemic parameters. Long-term intake of larger amounts of low glycemic index foods is related to higher HDL-cholesterol values [109] and a lower risk for developing CHD [84]. Based on these observations we recommend that the glycemic index be incorporated into diabetes exchange lists and nutrition teaching material to be an integral part of medical nutrition therapy. The recommended means for protein intake are fairly consistent across the international community. Our recommendations that protein provide 1216% of energy relate to the likelihood that excessive animal protein intake acts to sustain abnormal renal hyperfiltration that may contribute to development of diabetic nephropathy. Our clinical research indicates that substituting soy protein for animal protein significantly reduces hyperfiltration in type 1 diabetes [110]. Teixiera and colleagues [111] document that soy protein intake decreases albuminuria in type 2 diabetes. We suggest that reducing animal protein and increasing soy protein may have renoprotective effects at all stages of renal function. This hypothesis is still under examination. Soy protein intake has other health benefits, especially for diabetic individuals. Soy food intake improves serum lipid values [12,112], lowers CHD risk factors such as homocysteine and oxidation of LDL [113] and decreases risk for CHD in a variety of other ways [114]. There is not strong clinical evidence to make definitive recommendations about dietary fat. Intake of saturated and trans-fatty acids and cholesterol has adverse effects on serum lipoproteins and should be restricted [10]. To de-emphasize animal protein intake in favor of vegetable proteins such as soy we recommend that dietary cholesterol be restricted to 200 mg/day.

Conclusions
Medical nutrition therapy is the foundation upon which other diabetes management approaches are built. Fundamental nutrition goals are: blood glucose management, achieving and maintaining a desirable body weight, managing serum lipoproteins, reducing other risks for atherosclerotic cardiovascular disease and reducing risks for microvascular disease. Focusing on weight management is a very important nutrition task for obese diabetic individuals. A strong majority of the international diabetes community but not a consensus has these nutrition recommendations for diabetic individuals: attain and maintain a desirable body weight (BMI 25 kg/m2), have carbohydrate intakes of 50 60% of energy, limit monosaccharide and disaccharide intake from sources other than fruits and vegetables, use low glycemic index foods, have total dietary fiber intakes of 2535 g/day, have protein intakes of 1118% of energy, limit total dietary fat to 2530% of energy, have saturated plus trans fatty acid intakes of 10% of energy, polyunsaturated fat intakes of 9% of energy, and monounsaturated fat intakes of 9 14% of energy and have cholesterol intakes of 200 mg/d. These recommendations encourage use of whole grains, legumes, vegetables and fruits. Our evidence-based review using meta-analyses techniques largely support the strong majority recommendations of the international diabetes community. Strong RCTs support these recommendations: intake of carbohydrate of 55% or 55 65% of energy, dietary fiber intakes of 2550 g/d (1525 g/1000 kcal), total fat intakes of 30% of energy and incorporation of the glycemic index into diabetes counseling. There is very strong support for the recommendation that diabetic individuals achieve and maintain a desirable body weight with a BMI 25 kg/m2.

REFERENCES
1. Mokdad AH, Ford ES, Bowman BA, Nelson DE, Engelgau MM, Vinicor F, Marks JS: The continuing increase of diabetes in the US [Letter]. Diabetes Care 24:412, 2001. 2. King H, Aubert RE, Herman WH: Global burden of diabetes, 1995-2025; prevalence, numerical estimates, and projections. Diabetes Care 21:14141431, 1998. 3. American Diabetes Association: Evidence-based nutrition principles and recommendations for the treatment and prevention of diabetes and related complications. Diabetes Care 25:202212, 2002. 4. Nutrition Committee of the British Diabetic Associations Professional Advisory Committee: Dietary recommendations for people with diabetes: an update for the 1990s. Diabetic Med 9:189202, 1992.

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

13

Carbohydrate and Fiber Recommendations in Diabetes

5. National Nutrition Committee CDA: Guidelines for the nutritional management of diabetes mellitus in the new millennium: a position statement by the Canadian Diabetes Association. Can J Diabetes Care 23:5669, 1999. 6. Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD): 1. Recommendations for the nutritional management of patients with diabetes mellitus. Diabetes Nutr Metab 8:186189, 1995. 7. Singh RB, Rastogi SS, Rao PV, Das S, Madhu SV, Das AK, Sahay BK, Fuse SM, Beegom R, Sainani GS, Shah NA: Diet and lifestyle guidelines and desirable levels of risk factors for the prevention of diabetes and its vascular complications in Indians: a scientific statement of the International College of Nutrition. J Cardiovasc Risk 4:201208, 1997. 8. Kitamura S: Diet therapy and food exchange lists for diabetic patients. Diabetes Res Clin Pr 24:S233S240, 2001. 9. Silvis N: Nutrition recommendations for individuals with diabetes mellitus. S Afr Med J 81:162166, 1991. 10. Krauss RM, Eckel RH, Howard BV, Appel LJ, Daniels SR, Deckelbaum RJ, Erdman Jr JW, Kris-Etherton P, Goldberg IJ, Kotchen TA, Lichtenstein AH, Mitch WE, Mullis R, Robinson K, Wylie-Rosett J, St Jeor S, Suttie J, Tribble DL, Bazzarre TL: AHA Guidelines Revision 2000: A statement for healthcare professionals from the Nutrition Committee of the American Heart Association. Circulation 102:22842299, 2000. 11. Expert Panel on Detection, Valuation, and Treatment of High Blood Cholesterol in Adults: Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 285:24862497, 2001. 12. Anderson JW, Johnstone BM, Cook-Newell ME: Meta-analysis of effects of soy protein intake on serum lipids in humans. New Engl J Med 333:276282, 1995. 13. Anderson JW, Johnstone BM, Remley DT: Breast-feeding and cognitive function: a meta-analysis. Am J Clin Nutr 70:525535, 1999. 14. Anderson JW, Hanna TJ, Peng X, Kryscio RJ: Whole grain foods and heart disease risk. J Am Coll Nutr 2000;19:291S9S. 15. Rivellese A, Giacco A, Genovese S, Riccardi G, Pacioni D, Mattioli PL: Effect of dietary fibre on glucose control and serum lipoproteins in diabetic patients. Lancet 2:447450, 1980. 16. Rivellese A, Riccardi G, Giacco A, Postiglione A, Mastranzo P, Mattiolo PL: Reduction of risk factors for atherosclerosis in diabetic patients treated with a high-fiber diet. Prev Med 12:128 132, 1983. 17. Dodson PM, Pacy PJ, Bal P, Kubicki AJ, Fletcher RF, Taylor KG: A controlled trial of a high fiber, low fat and low sodium diet for mild hypertension in type 2 (non-insulin-dependent) diabetic patients. Diabetologia 27:522526, 1984. 18. Karlstrom B, Vessby B, Asp N, Boberg M, Gustafsson IB, Lithell H, Werner I: Effects of an increased content of cereal fiber in the diet of type II (non-insulin-dependent) diabetic patients. Diabetologia 26:272277, 1984. 19. Riccardi G, Rivellese A, Pacioni D, Genovese S, Mastranzo P, and Mancini M: Separate influence of dietary carbohydrate and fibre on the metabolic control in diabetes. Diabetologia 26,116 121, 1984. 20. Pacy PJ, Dodson PM, Fletcher RF: Effect of a high carbohydrate, low sodium and low fat diet in type 2 diabetics with moderate hypertension. Int J Obesity 10:4352, 1986. 21. Pacy PJ, Dodson PM, Taylor MP: The effect of a high fiber, low fat, low sodium diet on diabetics with intermittent claudication. Brit J Clin Pract 40:313317, 1986. 22. Hagander B, Asp NG, Efendic S, Nilsson-Ehle P, Schersten B: Dietary fiber decreases fasting blood glucose levels and plasma LDL concentration in noninsulin-dependent diabetes mellitus patients. Am J Clin Nutr 47:852858, 1988. 23. Venhaus A, Chantelau E: Self-selected unrefined and refined carbohydrate diets do not affect metabolic control in pumptreated diabetic patients. Diabetologia 3:153157, 2002. 24. Lafrance L, Rabasa-Lhoret R, Poisson D, Ducros F, Chiasson JL: Effects of different glycaemic index foods and dietary fibre intake on glycaemic control in type 1 diabetic patients on intensive insulin therapy. Diabetic Med 15:972978, 1998. 25. Chandalia M, Garg A, Lutjohann D, Von Bergmann K, Grundy SM, Brinkley LJ: Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. New Engl J Med 342: 13921398, 2000. 26. Anderson JW, Ward K: Long-term effects of high-carbohydrate, high-fiber diets on glucose and lipid metabolism: a preliminary report on patients with diabetes. Diabetes Care 1:7782, 1978. 27. Anderson JW, Ward K: High-carbohydrate, high-fiber diets for insulin-treated men with diabetes mellitus. Am J Clin Nutr 32: 23122321, 1979. 28. Simpson RW, Mann JI, Eaton J, Carter RD, Hockaday TDR: High-carbohydrate diets and insulin-dependent diabetics. Brit Med J 2:523525, 1979. 29. Simpson RW, Mann JI, Eaton J, Moore RA, Carter R, Hockaday TDR: Improved glucose control in maturity-onset diabetes treated with high-carbohydrate-modified fat diet. Brit Med J 1:1753 1756, 1979. 30. Anderson JW, Chen WJL, Sieling B: Hypolipidemic effects of high-carbohydrate, high-fiber diets. Metabolism 29:551558, 1980. 31. Hoffman CR, Fineberg SE, Howey DC, Clark CJ, Pronsky Z: Short-term effects of a high fiber, high carbohydrate diet in very obese diabetic individuals. Diabetes Care 5:605611, 1982. 32. Ward GM, Simpson RW, Simpson HCR, Naylor BA, Mann JI, Turner RC: Insulin receptor binding increased by high carbohydrate low fat diet in non-insulin dependent diabetics. Eur J Clin Invest 12:9398, 1982. 33. Taskinen M, Nikkila EA, Ollus A: Serum lipids and lipoproteins in insulin-dependent diabetic subjects during high-carbohydrate, high-fiber diet. Diabetes Care 6:224230, 1983. 34. Pacy PJ, Dodson PM, Kubicki AJ, Fletcher RF, Taylor KG: Comparison of the hypotensive and metabolic effects of bendrofluazide therapy and a high fiber, low fat, low sodium diet in diabetic subjects with hypertension. J Hypertens 2:215221, 1984. 35. Story L, Anderson JW, Chen WJL, Karounos D, Sieling B: Adherence to high-carbohydrate, high-fiber diets: long-term studies of non-obese diabetic men. J Am Diet Assoc 85:11051110, 1985. 36. Simpson RW, McDonald J, Wahlqvist ML, Balasz N, Sissons M, Atley L: Temporal study of metabolic changes when poorly

14

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

controlled noninsulin-dependent diabetics change from low to high carbohydrate and fiber diet. Am J Clin Nutr 48:104109, 1988. ODea K, Traianedes K, Ireland P, Niall M, Sadler J, Hopper J, De Luise M: The effects of diet differing in fat, carbohydrate, and fiber on carbohydrate and lipid metabolism in type II diabetes. J Am Diet Assoc 89, 10761086, 1989. Anderson JW, Zeigler JA, Deakins DA, Floore TL, Dillon DW, Wood CL, Oeltgen PR, Whitley RJ: Metabolic effects of highcarbohydrate, high-fiber diets for insulin-dependent diabetic individuals. Am J Clin Nutr 54:936943, 1991. Anderson JW, Konz EC: Obesity and disease management: Effects of weight loss on co-morbid conditions. Obes Res 9:326S 334S, 2001. Anderson JW: The role of dietary carbohydrate and fiber in the control of diabetes. In Stollerman GH (ed): Advances in Internal Medicine. Chicago: Year Book Medical Publishers, Inc., pp 6796, 1980. Marshall JA, Hamman RF, Baxter J: High-fat, low-carbohydrate diet and the etiology of non-insulin-dependent diabetes mellitus: The San Luis Valley Diabetes Study. Am J Epidemiol 134:590 603, 1991. Mensink RP, Katan MB: Effect of dietary fatty acids on serum lipids and lipoproteins: A meta-analysis of 27 trials. Arterioscler Thromb 12:911919, 1992. Anderson JW: Dietary fibre, complex carbohydrate and coronary artery disease. Can J Cardiol 11:55G62G, 1995. Anderson JW, Hanna TJ: Impact of nondigestible carbohydrates on serum lipoproteins and risk for cardiovascular disease. J Nutr 129:1457S1466S, 1999. Anderson JW, Allgood LD, Lawrence A, Altringer LA, Jerdack GR, Hengehold DA: Cholesterol-lowering effects of psyllium intake adjunctive to diet therapy in men and women with hypercholesterolemia: meta-analysis of 8 controlled trials. Am J Clin Nutr 71:472479, 2000. Anderson JW, Davidson MH, Blonde L, Brown WV, Howard WJ, Ginsberg H, Allgood LD, Weingand KW: Long-term cholesterol-lowering effects of psyllium as an adjunct to diet therapy in the treatment of hypercholesterolemia. Am J Clin Nutr 71: 14331438, 2000. Brown L, Rosner B, Willett WW, Sacks FM: Cholesterollowering effects of dietary fiber: a meta-analysis. Am J Clin Nutr 69:3042, 1999. Anderson JW: Dietary fiber prevents carbohydrate-induced hypertriglyceridemia. Curr Artheroscler Rep 2:536541, 2000. Howarth NC, Saltzman E, Roberts SB: Dietary fiber and weight regulation. Nutr Rev 59:129139, 2001. Anderson JW, Allgood LD, Turner C, Oelgten PR, Daggy BP: Effects of psyllium on glucose and serum lipid responses in men with type 2 diabetes and hypercholesterolemia. Am J Clin Nutr 70:466473, 1999. Anderson JW, Chen WJL, Karounos D, Jefferson B: Adherence to high-carbohydrate, high-fiber diets: Long-term studies of nonobese diabetic men. J Am Diet Assoc 85:11051110, 1985. Panel on Dietary Reference Intakes for Macronutrients and National Academy of Sciences: Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fatty Acids, Cholesterol, Protein, and Amino Acids. 9-5-2002. http://www4.nationalacademies. org.news.nsf/isbn Anderson JW, Akanji AO, Randles KM: Treatment of diabetes with high fiber diets. In Spiller GA (ed): Handbook of Dietary Fiber in Human Nutrition. Boca Raton, FL: CRC Press, pp 363390, 2001. Jenkins DJA, Kendall CWC, Augustin LSA, Martini MC, Axelsen M, Faulkner D, Vidgen E, Parker T, Lau H, Connelly PW, Teitel J, Singer W, Vandenbroucke AC, Leiter LA, Josse RG.: Effect of wheat bran on glycemic control and risk factors for cardiovascular disease in type 2 diabetes. Diabetes Care 25:1522 1528, 2002. Ford ES, Liu S: Glycemic index and serum high-density lipoprotein cholesterol concentration among us adults. Arch Intern Med 161:572576, 2001. Liu S, Manson JE, Stampfer MJ, Holmes MD, Hu FB, Hankinson SE, Willett WC: Dietary glycemic load assessed by foodfrequency questionnaire in relation to plasma high-densitylipoprotein cholesterol and fasting plasma triacylglycerols in postmenopausal women. Am J Clin Nutr 73:560566, 2001. Garg A, Grundy SM, and Unger RH: Comparison of effects of high and low carbohydrate diets on plasma lipoproteins and insulin sensitivity in patients with mild NIDDM. Diabetes 41, 12781285, 2000. Jenkins DJ, Kendall CW, Faulkner D Vidgen E, Trautwein EA, Parker TL, Marchie A, Koumbridis G, Lapsley KG, Josse RG, Leiter LA, Connelly PW: A dietary portfolio approach to cholesterol reduction: combined effects of plant sterols, vegetable proteins and viscous fibers in hypercholesterolemia. Metabolism 51:15961604, 2002. Wolever TM: The glycemic index. World Rev Nutr Diet 62:120 185, 1990. Jenkins DJA, Jenkins AL, Kendall CWC: Dietary therapy in type 2 diabetes mellitus: spreading the nutrient load. In Leroith D, Taylor S, Olefsky JM (eds): Diabetes Mellitus: a Fundamental and Clinical Text. Philadelphia: Lippincott Williams & Wilkins, pp 757765, 2000. Jenkins DJA, Wesson V, Wolever TM, Jenkins AL, Kalmusky J, Guidici J, Csima A, Josse RG, and Wong GS: Wholemeal versus wholegrain breads: proportion of whole or cracked grain and the glycaemic response. Br Med J 297:958960, 1988. Collier GR, Wolever TMS, Jenkins DJ: Concurrent ingestion of fat and reduction in starch content impairs carbohydrate tolerance to subsequent meals. Am J Clin Nutr 45:963969, 1987. Luscombe ND, Noakes M, Clifton PM: Diets high and low in glycemic index versus high monounsaturated fat diets: effects on glucose and lipid metabolism in NIDDM. Eur J Clin Nutr 53: 473478, 1999. Jarvi AE, Karlstrom BE, Granfeldt YE, Bjorck IE, Asp NG, Vessby BO: Improved glycemic control and lipid profile and normalized fibrinolytic activity on a low-glycemic index diet in type 2 diabetic patients. Diabetes Care 22:1018, 1999. Wolever TM, Jenkins DJ, Vuksan V, Jenkins AL, Buckley GC, Wong GS, Josse RG: Beneficial effect of a low glycaemic index diet in type 2 diabetes. Diabetic Med 9:451458, 1992. Wolever TM, Jenkins DJ, Vuksan V, Jenkins AL, Wong GS, Josse RG: Beneficial effect of low-glycemic index diet in overweight NIDDM subjects. Diabetes Care 15:562564, 1992.

53.

37.

54.

38.

39.

55.

40.

56.

41.

57.

42.

58.

43. 44.

45.

59. 60.

46.

61.

47.

62.

48. 49. 50.

63.

64.

51.

65.

52.

66.

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

15

Carbohydrate and Fiber Recommendations in Diabetes

67. Fontvieille AM, Rizkalla SW, Penfornis A, Acosta M, Bornet FR, Slama G: The use of low glycaemic index foods improves metabolic control of diabetic patients over five weeks. Diabetic Med 9:444450, 1992. 68. Brand JC, Colagiuri S, Crossman S, Allen A, Roberts DC, Truswell AS: Low-glycemic index foods improve long-term glycemic control in NIDDM. Diabetes Care 14:95101, 1991. 69. Calle-Pascual AL, Gomez V, Leon E, Bordiu E: Foods with low glycemic index do not improve glycemic control of both type 1 and type 2 diabetic patients after one month of therapy. Diabetes Metab 14:629633, 1998. 70. Fontvieille AM, Acosta M, Rizkalla SW, Bornet F, David P, Letanoux M, Tchobroutsky G, Slama G: A moderate switch from high to low glycaemic-index foods for 3 weeks improves the metabolic control of type 1 (IDDM) diabetic subjects. Diabetes Nutr Metab 1:139143, 1988. 71. Brand-Miller J: Glycemic index: scientific merit and utility for research and clinical practice. Presented American Diabetes Association. San Francisco CA. 6-15-2002. 72. Frost G, Wilding J, Beecham J: Dietary advice based on glycaemic index improves dietary profile and metabolic control in type 2 diabetes. Diabetic Med 11:397401, 1994. 73. Giacco R, Parillo M, Rivellese AA, Lasorella G, Giacco A, DEpiscopo L, Riccardi G: Long-term dietary treatment with increased amounts of fiber-rich low-glycemic index natural foods improves blood glucose control and reduces the number of hypoglycemic events in type 1 diabetic patients. Diabetes Care 23:14611466, 2000. 74. Komindr S, Ingsriswang S, Lerdvuthisopon N, Boontawee A: Effect of long-term intake of Asian food with different glycemic indices on diabetic control and protein conservation in type 2 diabetic patients. J Med Assoc Thailand 84:8597, 2001. 75. Gilbertson HR, Brand-Miller JC, Thorburn AW, Evans, Chondros P, Werther GA: The effect of flexible low glycemic index dietary advice versus measured carbohydrate exchange diets on glycemic control in children with type 1 diabetes. Diabetes Care 24:11371143, 2001. 76. Collier GR, Giudici S, Kalmusky J, Wolever T, Helman G, Wesson V, Ehrlich RM, Jenkins DJA: Low glycaemic index starchy foods improve glucose control and lower serum cholesterol in diabetic children. Diabetes Nutr Metab 1:1119, 1988. 77. Buyken AE, Toeller M, Heitkamp G, Karamanos B, Rottiers R, Muggeo M, Fuller JH, the EURODIAB IDDM Complications Study Group: Glycemic index in the diet of European outpatients with type 1 diabetes: relations to glycated hemoglobin and serum lipids. Am J Clin Nutr 73:574581, 2001. 78. Jenkins DJ, Kendall CW, Augustin LS, Franceschi S, Hamidi M, Marchie A, Jenkins AL, Axelsen M: Glycemic index: overview of implications in health and disease. Am J Clin Nutr 76:266S 273S, 2002. 79. Willett W, Manson J, Liu S: Glycemic index, glycemic load, and risk of type 2 diabetes. Am J Clin Nutr 76:274S280S, 2002. 80. Liu S, Manson JE, Buring JE, Stampfer MJ, Willett WC, Ridker PM: Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 75:492498, 2002. 81. Salmeron J, Manson JE, Stampfer MJ, Coldtiz GA, Wing AL, Willet WC: Dietary fiber, glycemic load, and risk of non-insulindependent diabetes mellitus in women. JAMA 277, 472477, 1997. Salmeron J, Ascherio A, Rimm EB, Colditz GA, Spiegelman D, Jenkins DJ, Stampfer MJ, Wing AL, Willett WC: Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care 20: 545550, 1997. Meyer KA, Kushi LH, Jacobs DR, Slavin J, Sellers TA, Folsom AR: Carbohydrates, dietary fiber, and incidence of type 2 diabetes in older women. Am J Clin Nutr 71:921930, 2000. Liu S, Willett WC, Stampfer MJ, Hu FB, Franz M, Sampson L, Hennekens CH, Manson JE: A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women. Am J Clin Nutr 71:14551461, 2000. Diabetes Australia: Food Choices for People with Diabetes. Sydney: Diabetes Australia, 2001. FAO/WHO Expert Committee: Carbohydrates in Human Nutrition: A Summary of the Joint FAO/WHO Expert Consultation, 1997. Rome: Food and Agriculture Organization (United Nations), 1997. Mann J, Lean M, Toeller M, Slama G, Uusitupa M, Vessby B: Recommendations for the nutritional management of patients with diabetes mellitus. Eur J Clin Nutr 54:353355, 2000. Perlstein R, Willcox J, Hines C, Milosavljevic M: Glycaemic index in diabetes management. Austral J Nutr Dietet 54:5763, 1997. Pi-Sunyer FX: Glycemic index and disease. Am J Clin Nutr 76:290S298S, 2002. Gilbertson HR, Thorburn AW, Brand-Miller JC, Chondros P, Werther GA: Effect of low-glycemic-index dietary advice on dietary quality and food choice in children with type 1 diabetes. Am J Clin Nutr 77:8390, 2003. Slavin JL, Jacobs DR, Marquart L: Whole-grain consumption and chronic disease: protective mechanisms. Nutr Cancer 27:1421, 1997. Truswell AS: Cereal grains and coronary heart disease. Eur J Clin Nutr 56:114, 2002. Ludwig DS, Pereira MA, Kroenke CH, Hilner JE, Van Horn L, Slattery ML, Jacobs Jr DR: Dietary fiber, weight gain, and cardiovascular disease risk factors in young adults. JAMA 282: 15391546. Cleveland LE, Moshfegh AJ, Albertson AM, Goldman JD: Dietary intake of whole grains. J Am Coll Nutr 19:331S338S, 2000. Mann JI, Lewis-Barned NJ: Dietary management of diabetes mellitus in Europe and North America. In Alberti KGMM, Zimmet P, DeFronzo RA, Keen H (eds): International Textbook of Diabetes Mellitus. New York: John Wiley & Sons, Ltd., pp 759771, 1997. Pan XR. Dietary management of diabetes mellitus in China. In Alberti KGMM, Zimmet P, DeFronzo RA, Keen H (eds): International Textbook of Diabetes Mellitus. New York: John Wiley & Sons, Ltd., pp 791793, 1997. Anderson JW, Kendall CWC, Jenkins DJA: Importance of weight management in type 2 diabetes: review with meta-analysis of clinical studies. J Am Coll Nutr 22:331339, 2003. Knowler WC, Pettitt D, Savage PJ, Bennett P: Diabetes incidence

82.

83.

84.

85. 86.

87.

88.

89. 90.

91.

92. 93.

94.

95.

96.

97.

98.

16

VOL. 23, NO. 1

Carbohydrate and Fiber Recommendations in Diabetes

in Pima Indians: contributions of obesity and parental diabetes. Am J Epidemiol 113:144156, 1981. Colditz GA, Willett WC, Stampfer MJ, Manson JE, Hennekens CH, Arky RA, Speizer FE: Weight as a risk factor for clinical diabetes in women. Am J Epidemiol 132:501513, 1990. Wolf AM: Current estimates of the economic cost of obesity in the United States. Obes Res 6:97106, 1998. Gu K, Cowie CC, and Harris MI: Diabetes and decline in heart disease mortality in US adults. JAMA 281:12911297, 1999. OKeefe JH, Miles JM, Harris WH, Moe RM, McCallister BD: Improving the adverse cardiovascular prognosis in type 2 diabetes. Mayo Clin Proc 74:171180, 1999. Ramachandran A, Viswanathan M: Dietary management of diabetes mellitus in India and South East Asia. In Alberti KGMM, Zimmet P, DeFronzo RA, Keen H (eds): International Textbook of Diabetes Mellitus. New York: John Wiley & Sons, Ltd., pp 773777, 1997. Food and Drug Administration: Wholegrain Foods Authoritative Statement Claim Notification. Docket 99P-2209. Washington, DC: US FDA, 1999. US Department of Agriculture (USDA) and US Department of Health and Human Services: Dietary Guidelines for Americans. Washington, DC: USDA. Home and Garden Bulletin 232, pp1 215, 2000. Burton-Freeman B: Dietary fiber and energy regulation. J Nutr 130:272S275S, 2000. Jenkins DJA, Wolever TMS, Taylor RH, Barker, H, Fielden H, Baldwin JM, Bowling JM, Newman, HC, Jenkins AL, Goff DV: Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr 34:362366, 1981. 108. Foster-Powell K, Miller JB: International tables of glycemic index. Am J Clin Nutr 62:871S890S, 1995. 109. Frost G, Leeds AA, Dore CJ, Madeiros S, Brading S, Dornhorst A: Glycaemic index as a determinant of serum HDL-cholesterol concentration. Lancet 353:10451048, 1999. 110. Stephenson TJ: Therapeutic Benefits of a Soy Protein Rich Diet in the Prevention and Treatment of Nephropathy in Young Persons with Type 1, Insulin-Dependent, Diabetes Mellitus. Lexington: University of Kentucky, pp 1238, 2001. 111. Teixeira SR, Tappenden KA, Marshall WA, Carson LA, Ringenberg M, Erdman JW: Effects of soy protein on diabetic nephropathy and blood lipids in type 2 diabetes mellitus [Abstract]. Program, 4th International Symposium on the Role of Soy in Preventing and Treating Chronic Disease 1:36, 2001. 112. Hermansen K, Soondergaard M, Hoie L, Carstensen M, Brock B: Beneficial effects of a soy-based dietary supplement on lipid levels and cardiovascular risk markers in type 2 diabetic subjects. Diabetes Care 24:228233, 2001. 113. Jenkins DJA, Kendall CWC, Jackson CJ, Connelly PW, Parker T, Faulkner D, Vidgen E, Cunnane SC, Leiter LA, Josse RG: Effect of high- and low-isoflavone soyfoods on blood lipids, oxidized LDL, homocysteine, and blood pressure in hyperlipidemic men and women. Am J Clin Nutr 76:365372, 2002. 114. Anderson JW, Hanna TJ: Soy foods and health promotion. In: Watson T (ed): Vegetables, Fruits, and Herbs in Health Promotion. Boca Raton, FL: CRC Press, pp11734, 2001.

99.

100. 101. 102.

103.

104.

105.

106. 107.

Received November 27, 2002; revision accepted May 13, 2003

JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION

17